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Published in: The Journal of Headache and Pain 1/2017

Open Access 01-12-2017 | Research article

Habituation of laser-evoked potentials by migraine phase: a blinded longitudinal study

Authors: Martin Uglem, Petter Moe Omland, Marit Stjern, Gøril Bruvik Gravdahl, Trond Sand

Published in: The Journal of Headache and Pain | Issue 1/2017

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Abstract

Background

Migraineurs seem to have cyclic variations in cortical excitability in several neurophysiological modalities. Laser-evoked potentials (LEP) are of particular interest in migraine because LEP specifically targets pain pathways, and studies have reported different LEP-changes both between and during headaches. Our primary aim was to explore potential cyclic variations in LEP amplitude and habituation in more detail with a blinded longitudinal study design.

Methods

We compared N1 and N2P2 amplitudes and habituation between two blocks of laser stimulations to the dorsal hand, obtained from 49 migraineurs with four sessions each. We used migraine diaries to categorize sessions as interictal (> one day from previous and to next attack), preictal (< one day before the attack), ictal or postictal (< one day after the attack). Also, we compared 29 interictal recordings from the first session to 30 controls.

Results

N1 and N2P2 amplitudes and habituation did not differ between preictal, interictal and postictal phase sessions, except for a post hoc contrast that showed deficient ictal habituation of N1. Habituation is present and similar in migraineurs in the interictal phase and controls.

Conclusions

Hand-evoked LEP amplitudes and habituation were mainly invariable between migraine phases, but this matter needs further study. Because hand-evoked LEP-habituation was similar in migraineurs and controls, the present findings contradict several previous LEP studies. Pain-evoked cerebral responses are normal and show normal habituation in migraine.
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Literature
1.
go back to reference Maniyar FH, Sprenger T, Monteith T, Schankin CJ, Goadsby PJ (2015) The premonitory phase of migraine--what can we learn from it? Headache 55:609–620CrossRefPubMed Maniyar FH, Sprenger T, Monteith T, Schankin CJ, Goadsby PJ (2015) The premonitory phase of migraine--what can we learn from it? Headache 55:609–620CrossRefPubMed
3.
go back to reference Schulte LH, May A (2016) The migraine generator revisited: continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain 139:1987–1993CrossRefPubMed Schulte LH, May A (2016) The migraine generator revisited: continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain 139:1987–1993CrossRefPubMed
4.
go back to reference Sand T, Zhitniy N, White LR, Stovner LJ (2008) Brainstem auditory-evoked potential habituation and intensity-dependence related to serotonin metabolism in migraine: a longitudinal study. Clin Neurophysiol 119:1190–1200CrossRefPubMed Sand T, Zhitniy N, White LR, Stovner LJ (2008) Brainstem auditory-evoked potential habituation and intensity-dependence related to serotonin metabolism in migraine: a longitudinal study. Clin Neurophysiol 119:1190–1200CrossRefPubMed
5.
go back to reference Sand T, Zhitniy N, White LR, Stovner LJ (2008) Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin Neurophysiol 119:1020–1027CrossRefPubMed Sand T, Zhitniy N, White LR, Stovner LJ (2008) Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin Neurophysiol 119:1020–1027CrossRefPubMed
7.
go back to reference Harriott AM, Schwedt TJ (2014) Migraine is associated with altered processing of sensory stimuli. Curr Pain Headache Rep 18:458CrossRefPubMed Harriott AM, Schwedt TJ (2014) Migraine is associated with altered processing of sensory stimuli. Curr Pain Headache Rep 18:458CrossRefPubMed
8.
go back to reference Schulte LH, May A (2016) Functional Neuroimaging in Migraine: Chances and Challenges. Headache 56:1474–1481CrossRefPubMed Schulte LH, May A (2016) Functional Neuroimaging in Migraine: Chances and Challenges. Headache 56:1474–1481CrossRefPubMed
9.
go back to reference de Tommaso M, Ambrosini A, Brighina F, Coppola G, Perrotta A, Pierelli F, Sandrini G, Valeriani M, Marinazzo D, Stramaglia S, Schoenen J (2014) Altered processing of sensory stimuli in patients with migraine. Nat Rev Neurol 10:144–155CrossRefPubMed de Tommaso M, Ambrosini A, Brighina F, Coppola G, Perrotta A, Pierelli F, Sandrini G, Valeriani M, Marinazzo D, Stramaglia S, Schoenen J (2014) Altered processing of sensory stimuli in patients with migraine. Nat Rev Neurol 10:144–155CrossRefPubMed
10.
go back to reference Cruccu G, Sommer C, Anand P, Attal N, Baron R, Garcia-Larrea L, Haanpaa M, Jensen TS, Serra J, Treede RD (2010) EFNS guidelines on neuropathic pain assessment: revised 2009. Eur J Neurol 17:1010–1018CrossRefPubMed Cruccu G, Sommer C, Anand P, Attal N, Baron R, Garcia-Larrea L, Haanpaa M, Jensen TS, Serra J, Treede RD (2010) EFNS guidelines on neuropathic pain assessment: revised 2009. Eur J Neurol 17:1010–1018CrossRefPubMed
11.
go back to reference Garcia-Larrea L, Frot M, Valeriani M (2003) Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33:279–292CrossRefPubMed Garcia-Larrea L, Frot M, Valeriani M (2003) Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33:279–292CrossRefPubMed
12.
go back to reference Treede RD, Lorenz J, Baumgartner U (2003) Clinical usefulness of laser-evoked potentials. Neurophysiol Clin 33:303–314CrossRefPubMed Treede RD, Lorenz J, Baumgartner U (2003) Clinical usefulness of laser-evoked potentials. Neurophysiol Clin 33:303–314CrossRefPubMed
13.
go back to reference Bromm B, Treede RD (1984) Nerve fibre discharges, cerebral potentials and sensations induced by CO2 laser stimulation. Hum Neurobiol 3:33–40PubMed Bromm B, Treede RD (1984) Nerve fibre discharges, cerebral potentials and sensations induced by CO2 laser stimulation. Hum Neurobiol 3:33–40PubMed
14.
go back to reference Carmon A, Mor J, Goldberg J (1976) Evoked cerebral responses to noxious thermal stimuli in humans. Exp Brain Res 25:103–107CrossRefPubMed Carmon A, Mor J, Goldberg J (1976) Evoked cerebral responses to noxious thermal stimuli in humans. Exp Brain Res 25:103–107CrossRefPubMed
15.
go back to reference Iannetti GD, Zambreanu L, Cruccu G, Tracey I (2005) Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131:199–208CrossRefPubMed Iannetti GD, Zambreanu L, Cruccu G, Tracey I (2005) Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131:199–208CrossRefPubMed
16.
go back to reference Valentini E, Hu L, Chakrabarti B, Hu Y, Aglioti SM, Iannetti GD (2012) The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli. NeuroImage 59:1571–1581CrossRefPubMed Valentini E, Hu L, Chakrabarti B, Hu Y, Aglioti SM, Iannetti GD (2012) The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli. NeuroImage 59:1571–1581CrossRefPubMed
17.
go back to reference Valeriani M, de Tommaso M, Restuccia D, Le Pera D, Guido M, Iannetti GD, Libro G, Truini A, Di Trapani G, Puca F, Tonali P, Cruccu G (2003) Reduced habituation to experimental pain in migraine patients: a CO(2) laser evoked potential study. Pain 105:57–64CrossRefPubMed Valeriani M, de Tommaso M, Restuccia D, Le Pera D, Guido M, Iannetti GD, Libro G, Truini A, Di Trapani G, Puca F, Tonali P, Cruccu G (2003) Reduced habituation to experimental pain in migraine patients: a CO(2) laser evoked potential study. Pain 105:57–64CrossRefPubMed
18.
go back to reference de Tommaso M, Valeriani M, Sardaro M, Serpino C, Fruscolo OD, Vecchio E, Cerbo R, Livrea P (2009) Pain perception and laser evoked potentials during menstrual cycle in migraine. J Headache Pain 10:423–429CrossRefPubMedPubMedCentral de Tommaso M, Valeriani M, Sardaro M, Serpino C, Fruscolo OD, Vecchio E, Cerbo R, Livrea P (2009) Pain perception and laser evoked potentials during menstrual cycle in migraine. J Headache Pain 10:423–429CrossRefPubMedPubMedCentral
19.
go back to reference de Tommaso M, Libro G, Guido M, Losito L, Lamberti P, Livrea P (2005) Habituation of single CO2 laser-evoked responses during interictal phase of migraine. J Headache Pain 6:195–198CrossRefPubMedPubMedCentral de Tommaso M, Libro G, Guido M, Losito L, Lamberti P, Livrea P (2005) Habituation of single CO2 laser-evoked responses during interictal phase of migraine. J Headache Pain 6:195–198CrossRefPubMedPubMedCentral
20.
go back to reference Di Clemente L, Puledda F, Biasiotta A, Vigano A, Vicenzini E, Truini A, Cruccu G, Di Piero V (2013) Topiramate modulates habituation in migraine: evidences from nociceptive responses elicited by laser evoked potentials. J Headache Pain 14:25CrossRefPubMedPubMedCentral Di Clemente L, Puledda F, Biasiotta A, Vigano A, Vicenzini E, Truini A, Cruccu G, Di Piero V (2013) Topiramate modulates habituation in migraine: evidences from nociceptive responses elicited by laser evoked potentials. J Headache Pain 14:25CrossRefPubMedPubMedCentral
21.
go back to reference de Tommaso M, Lo Sito L, Di Fruscolo O, Sardaro M, Pia Prudenzano M, Lamberti P, Livrea P (2005) Lack of habituation of nociceptive evoked responses and pain sensitivity during migraine attack. Clin Neurophysiol 116:1254–1264CrossRefPubMed de Tommaso M, Lo Sito L, Di Fruscolo O, Sardaro M, Pia Prudenzano M, Lamberti P, Livrea P (2005) Lack of habituation of nociceptive evoked responses and pain sensitivity during migraine attack. Clin Neurophysiol 116:1254–1264CrossRefPubMed
22.
go back to reference Vecchio E, Ricci K, Montemurno A, Delussi M, Invitto S, de Tommaso M (2016) Effects of left primary motor and dorsolateral prefrontal cortex transcranial direct current stimulation on laser-evoked potentials in migraine patients and normal subjects. Neurosci Lett 626:149–157CrossRefPubMed Vecchio E, Ricci K, Montemurno A, Delussi M, Invitto S, de Tommaso M (2016) Effects of left primary motor and dorsolateral prefrontal cortex transcranial direct current stimulation on laser-evoked potentials in migraine patients and normal subjects. Neurosci Lett 626:149–157CrossRefPubMed
23.
go back to reference de Tommaso M, Guido M, Libro G, Losito L, Sciruicchio V, Monetti C, Puca F (2002) Abnormal brain processing of cutaneous pain in migraine patients during the attack. Neurosci Lett 333:29–32CrossRefPubMed de Tommaso M, Guido M, Libro G, Losito L, Sciruicchio V, Monetti C, Puca F (2002) Abnormal brain processing of cutaneous pain in migraine patients during the attack. Neurosci Lett 333:29–32CrossRefPubMed
24.
go back to reference de Tommaso M, Guido M, Libro G, Losito L, Difruscolo O, Puca F, Specchio LM, Carella A (2004) Topographic and dipolar analysis of laser-evoked potentials during migraine attack. Headache 44:947–960CrossRefPubMed de Tommaso M, Guido M, Libro G, Losito L, Difruscolo O, Puca F, Specchio LM, Carella A (2004) Topographic and dipolar analysis of laser-evoked potentials during migraine attack. Headache 44:947–960CrossRefPubMed
25.
go back to reference Hullemann P, von der Brelie C, Manthey G, Dusterhoft J, Helmers AK, Synowitz M, Baron R (2017) Reduced laser-evoked potential habituation detects abnormal central pain processing in painful radiculopathy patients. Eur J Pain 21:918–926CrossRefPubMed Hullemann P, von der Brelie C, Manthey G, Dusterhoft J, Helmers AK, Synowitz M, Baron R (2017) Reduced laser-evoked potential habituation detects abnormal central pain processing in painful radiculopathy patients. Eur J Pain 21:918–926CrossRefPubMed
26.
go back to reference de Tommaso M, Federici A, Santostasi R, Calabrese R, Vecchio E, Lapadula G, Iannone F, Lamberti P, Livrea P (2011) Laser-evoked potentials habituation in fibromyalgia. J Pain 12:116–124CrossRefPubMed de Tommaso M, Federici A, Santostasi R, Calabrese R, Vecchio E, Lapadula G, Iannone F, Lamberti P, Livrea P (2011) Laser-evoked potentials habituation in fibromyalgia. J Pain 12:116–124CrossRefPubMed
27.
go back to reference Valeriani M, Sestito A, Le Pera D, De Armas L, Infusino F, Maiese T, Sgueglia GA, Tonali PA, Crea F, Restuccia D, Lanza GA (2005) Abnormal cortical pain processing in patients with cardiac syndrome X. Eur Heart J 26:975–982CrossRefPubMed Valeriani M, Sestito A, Le Pera D, De Armas L, Infusino F, Maiese T, Sgueglia GA, Tonali PA, Crea F, Restuccia D, Lanza GA (2005) Abnormal cortical pain processing in patients with cardiac syndrome X. Eur Heart J 26:975–982CrossRefPubMed
29.
go back to reference Di Clemente L, Coppola G, Magis D, Fumal A, De Pasqua V, Schoenen J (2005) Nociceptive blink reflex and visual evoked potential habituations are correlated in migraine. Headache 45:1388–1393CrossRefPubMed Di Clemente L, Coppola G, Magis D, Fumal A, De Pasqua V, Schoenen J (2005) Nociceptive blink reflex and visual evoked potential habituations are correlated in migraine. Headache 45:1388–1393CrossRefPubMed
30.
go back to reference Stankewitz A, Schulz E, May A (2013) Neuronal correlates of impaired habituation in response to repeated trigemino-nociceptive but not to olfactory input in migraineurs: an fMRI study. Cephalalgia 33:256–265CrossRefPubMed Stankewitz A, Schulz E, May A (2013) Neuronal correlates of impaired habituation in response to repeated trigemino-nociceptive but not to olfactory input in migraineurs: an fMRI study. Cephalalgia 33:256–265CrossRefPubMed
31.
go back to reference Katsarava Z, Giffin N, Diener HC, Kaube H (2003) Abnormal habituation of 'nociceptive' blink reflex in migraine--evidence for increased excitability of trigeminal nociception. Cephalalgia 23:814–819CrossRefPubMed Katsarava Z, Giffin N, Diener HC, Kaube H (2003) Abnormal habituation of 'nociceptive' blink reflex in migraine--evidence for increased excitability of trigeminal nociception. Cephalalgia 23:814–819CrossRefPubMed
32.
go back to reference Omland PM, Uglem M, Hagen K, Linde M, Tronvik E, Sand T (2016) Visual evoked potentials in migraine: Is the "neurophysiological hallmark" concept still valid? Clin Neurophysiol 127:810–816CrossRefPubMed Omland PM, Uglem M, Hagen K, Linde M, Tronvik E, Sand T (2016) Visual evoked potentials in migraine: Is the "neurophysiological hallmark" concept still valid? Clin Neurophysiol 127:810–816CrossRefPubMed
34.
go back to reference De Marinis M, Pujia A, Natale L, D'Arcangelo E, Accornero N (2003) Decreased habituation of the R2 component of the blink reflex in migraine patients. Clin Neurophysiol 114:889–893CrossRefPubMed De Marinis M, Pujia A, Natale L, D'Arcangelo E, Accornero N (2003) Decreased habituation of the R2 component of the blink reflex in migraine patients. Clin Neurophysiol 114:889–893CrossRefPubMed
35.
go back to reference Sand T, Vingen JV (2000) Visual, long-latency auditory and brainstem auditory evoked potentials in migraine: relation to pattern size, stimulus intensity, sound and light discomfort thresholds and pre-attack state. Cephalalgia 20:804–820CrossRefPubMed Sand T, Vingen JV (2000) Visual, long-latency auditory and brainstem auditory evoked potentials in migraine: relation to pattern size, stimulus intensity, sound and light discomfort thresholds and pre-attack state. Cephalalgia 20:804–820CrossRefPubMed
36.
go back to reference Chen WT, Wang SJ, Fuh JL, Lin CP, Ko YC, Lin YY (2009) Peri-ictal normalization of visual cortex excitability in migraine: an MEG study. Cephalalgia 29:1202–1211CrossRefPubMed Chen WT, Wang SJ, Fuh JL, Lin CP, Ko YC, Lin YY (2009) Peri-ictal normalization of visual cortex excitability in migraine: an MEG study. Cephalalgia 29:1202–1211CrossRefPubMed
37.
go back to reference Judit A, Sandor PS, Schoenen J (2000) Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia 20:714–719CrossRefPubMed Judit A, Sandor PS, Schoenen J (2000) Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia 20:714–719CrossRefPubMed
38.
go back to reference Coppola G, Curra A, Di Lorenzo C, Parisi V, Gorini M, Sava SL, Schoenen J, Pierelli F (2010) Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol 10:126CrossRefPubMedPubMedCentral Coppola G, Curra A, Di Lorenzo C, Parisi V, Gorini M, Sava SL, Schoenen J, Pierelli F (2010) Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol 10:126CrossRefPubMedPubMedCentral
39.
go back to reference Coppola G, Iacovelli E, Bracaglia M, Serrao M, Di Lorenzo C, Pierelli F (2013) Electrophysiological correlates of episodic migraine chronification: evidence for thalamic involvement. J Headache Pain 14:76CrossRefPubMedPubMedCentral Coppola G, Iacovelli E, Bracaglia M, Serrao M, Di Lorenzo C, Pierelli F (2013) Electrophysiological correlates of episodic migraine chronification: evidence for thalamic involvement. J Headache Pain 14:76CrossRefPubMedPubMedCentral
40.
go back to reference Kalita J, Bhoi SK, Misra UK (2014) Is lack of habituation of evoked potential a biological marker of migraine? Clin J Pain 30:724–729CrossRefPubMed Kalita J, Bhoi SK, Misra UK (2014) Is lack of habituation of evoked potential a biological marker of migraine? Clin J Pain 30:724–729CrossRefPubMed
41.
go back to reference Chen WT, Wang SJ, Fuh JL, Lin CP, Ko YC, Lin YY (2011) Persistent ictal-like visual cortical excitability in chronic migraine. Pain 152:254–258CrossRefPubMed Chen WT, Wang SJ, Fuh JL, Lin CP, Ko YC, Lin YY (2011) Persistent ictal-like visual cortical excitability in chronic migraine. Pain 152:254–258CrossRefPubMed
42.
go back to reference Kropp P, Gerber WD (2005) Slow cortical potentials in migraine. Predictive value and possible novel therapeutic strategies to prevent an attack. Funct Neurol 20:193–197PubMed Kropp P, Gerber WD (2005) Slow cortical potentials in migraine. Predictive value and possible novel therapeutic strategies to prevent an attack. Funct Neurol 20:193–197PubMed
43.
go back to reference Siniatchkin M, Averkina N, Andrasik F, Stephani U, Gerber WD (2006) Neurophysiological reactivity before a migraine attack. Neurosci Lett 400:121–124CrossRefPubMed Siniatchkin M, Averkina N, Andrasik F, Stephani U, Gerber WD (2006) Neurophysiological reactivity before a migraine attack. Neurosci Lett 400:121–124CrossRefPubMed
44.
go back to reference Kropp P, Gerber WD (1995) Contingent negative variation during migraine attack and interval: evidence for normalization of slow cortical potentials during the attack. Cephalalgia 15:123–128 discussion 178-129CrossRefPubMed Kropp P, Gerber WD (1995) Contingent negative variation during migraine attack and interval: evidence for normalization of slow cortical potentials during the attack. Cephalalgia 15:123–128 discussion 178-129CrossRefPubMed
45.
go back to reference Evers S, Quibeldey F, Grotemeyer KH, Suhr B, Husstedt IW (1999) Dynamic changes of cognitive habituation and serotonin metabolism during the migraine interval. Cephalalgia 19:485–491CrossRefPubMed Evers S, Quibeldey F, Grotemeyer KH, Suhr B, Husstedt IW (1999) Dynamic changes of cognitive habituation and serotonin metabolism during the migraine interval. Cephalalgia 19:485–491CrossRefPubMed
48.
go back to reference Headache Classification Subcommittee of the International Headache Society (2004) The International Classification of Headache Disorders: 2nd edition. Cephalalgia 24 Suppl 1:9–160 Headache Classification Subcommittee of the International Headache Society (2004) The International Classification of Headache Disorders: 2nd edition. Cephalalgia 24 Suppl 1:9–160
49.
go back to reference Odegard SS, Omland PM, Nilsen KB, Stjern M, Gravdahl GB, Sand T (2015) The effect of sleep restriction on laser evoked potentials, thermal sensory and pain thresholds and suprathreshold pain in healthy subjects. Clin Neurophysiol 126:1979–1987CrossRefPubMed Odegard SS, Omland PM, Nilsen KB, Stjern M, Gravdahl GB, Sand T (2015) The effect of sleep restriction on laser evoked potentials, thermal sensory and pain thresholds and suprathreshold pain in healthy subjects. Clin Neurophysiol 126:1979–1987CrossRefPubMed
50.
go back to reference Iannetti GD, Leandri M, Truini A, Zambreanu L, Cruccu G, Tracey I (2004) Adelta nociceptor response to laser stimuli: selective effect of stimulus duration on skin temperature, brain potentials and pain perception. Clin Neurophysiol 115:2629–2637CrossRefPubMed Iannetti GD, Leandri M, Truini A, Zambreanu L, Cruccu G, Tracey I (2004) Adelta nociceptor response to laser stimuli: selective effect of stimulus duration on skin temperature, brain potentials and pain perception. Clin Neurophysiol 115:2629–2637CrossRefPubMed
51.
go back to reference Isak B, Tankisi H, Johnsen B, Pugdahl K, Finnerup NB, Fuglsang-Frederiksen A (2016) Laser and somatosensory evoked potentials in amyotrophic lateral sclerosis. Clin Neurophysiol 127:3322–3328CrossRefPubMed Isak B, Tankisi H, Johnsen B, Pugdahl K, Finnerup NB, Fuglsang-Frederiksen A (2016) Laser and somatosensory evoked potentials in amyotrophic lateral sclerosis. Clin Neurophysiol 127:3322–3328CrossRefPubMed
52.
go back to reference Di Stefano G, Celletti C, Baron R, Castori M, Di Franco M, La Cesa S, Leone C, Pepe A, Cruccu G, Truini A, Camerota F (2016) Central sensitization as the mechanism underlying pain in joint hypermobility syndrome/Ehlers-Danlos syndrome, hypermobility type. Eur J Pain 20:1319–1325CrossRefPubMed Di Stefano G, Celletti C, Baron R, Castori M, Di Franco M, La Cesa S, Leone C, Pepe A, Cruccu G, Truini A, Camerota F (2016) Central sensitization as the mechanism underlying pain in joint hypermobility syndrome/Ehlers-Danlos syndrome, hypermobility type. Eur J Pain 20:1319–1325CrossRefPubMed
53.
go back to reference Cruccu G, Aminoff MJ, Curio G, Guerit JM, Kakigi R, Mauguiere F, Rossini PM, Treede RD, Garcia-Larrea L (2008) Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119:1705–1719CrossRefPubMed Cruccu G, Aminoff MJ, Curio G, Guerit JM, Kakigi R, Mauguiere F, Rossini PM, Treede RD, Garcia-Larrea L (2008) Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119:1705–1719CrossRefPubMed
54.
go back to reference Garcia-Larrea L, Peyron R, Laurent B, Mauguiere F (1997) Association and dissociation between laser-evoked potentials and pain perception. Neuroreport 8:3785–3789CrossRefPubMed Garcia-Larrea L, Peyron R, Laurent B, Mauguiere F (1997) Association and dissociation between laser-evoked potentials and pain perception. Neuroreport 8:3785–3789CrossRefPubMed
55.
go back to reference Lefaucheur JP, Debray S, Jarry G (2001) Laser evoked potentials using the Nd:YAG laser. Muscle Nerve 24:496–501CrossRefPubMed Lefaucheur JP, Debray S, Jarry G (2001) Laser evoked potentials using the Nd:YAG laser. Muscle Nerve 24:496–501CrossRefPubMed
56.
go back to reference Treede RD, Meyer RA, Raja SN, Campbell JN (1995) Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J Physiol 483(Pt 3):747–758CrossRefPubMedPubMedCentral Treede RD, Meyer RA, Raja SN, Campbell JN (1995) Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J Physiol 483(Pt 3):747–758CrossRefPubMedPubMedCentral
57.
go back to reference Truini A, Galeotti F, Romaniello A, Virtuoso M, Iannetti GD, Cruccu G (2005) Laser-evoked potentials: normative values. Clin Neurophysiol 116:821–826CrossRefPubMed Truini A, Galeotti F, Romaniello A, Virtuoso M, Iannetti GD, Cruccu G (2005) Laser-evoked potentials: normative values. Clin Neurophysiol 116:821–826CrossRefPubMed
58.
go back to reference de Tommaso M, Ricci K, Montemurno A, Vecchio E (2017) Age-related changes in laser-evoked potentials following trigeminal and hand stimulation in healthy subjects. Eur J Pain 21:1087–1097CrossRefPubMed de Tommaso M, Ricci K, Montemurno A, Vecchio E (2017) Age-related changes in laser-evoked potentials following trigeminal and hand stimulation in healthy subjects. Eur J Pain 21:1087–1097CrossRefPubMed
59.
go back to reference Bromm B, Lorenz J (1998) Neurophysiological evaluation of pain. Electroencephalogr Clin Neurophysiol 107:227–253CrossRefPubMed Bromm B, Lorenz J (1998) Neurophysiological evaluation of pain. Electroencephalogr Clin Neurophysiol 107:227–253CrossRefPubMed
60.
go back to reference Beydoun A, Morrow TJ, Shen JF, Casey KL (1993) Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr Clin Neurophysiol 88:173–181CrossRefPubMed Beydoun A, Morrow TJ, Shen JF, Casey KL (1993) Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr Clin Neurophysiol 88:173–181CrossRefPubMed
61.
go back to reference Lorenz J, Garcia-Larrea L (2003) Contribution of attentional and cognitive factors to laser evoked brain potentials. Neurophysiol Clin 33:293–301CrossRefPubMed Lorenz J, Garcia-Larrea L (2003) Contribution of attentional and cognitive factors to laser evoked brain potentials. Neurophysiol Clin 33:293–301CrossRefPubMed
62.
go back to reference Sand T, Zhitniy N, Nilsen KB, Helde G, Hagen K, Stovner LJ (2008) Thermal pain thresholds are decreased in the migraine preattack phase. Eur J Neurol 15:1199–1205CrossRefPubMed Sand T, Zhitniy N, Nilsen KB, Helde G, Hagen K, Stovner LJ (2008) Thermal pain thresholds are decreased in the migraine preattack phase. Eur J Neurol 15:1199–1205CrossRefPubMed
63.
go back to reference Kunde V, Treede RD (1993) Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. Electroencephalogr Clin Neurophysiol 88:280–289CrossRefPubMed Kunde V, Treede RD (1993) Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. Electroencephalogr Clin Neurophysiol 88:280–289CrossRefPubMed
64.
go back to reference StataCorp (2013) intreg - interval regression. In: Stata 13 base reference manual, Stata Press. College Station, TX StataCorp (2013) intreg - interval regression. In: Stata 13 base reference manual, Stata Press. College Station, TX
65.
go back to reference Smithson M, Merkle EC (2013) Censoring and Truncation. In: Generalized Linear Models for Categorical and Continuous Limited Dependent Variables. CRC Press, Boca Raton, FL Smithson M, Merkle EC (2013) Censoring and Truncation. In: Generalized Linear Models for Categorical and Continuous Limited Dependent Variables. CRC Press, Boca Raton, FL
66.
go back to reference Rabe-Hesketh S, Skrondal A (2012) Multilevel and longitudinal modeling using Stata : Vol. 1 : Continuous responses. Stata Press, College Station, Tex Rabe-Hesketh S, Skrondal A (2012) Multilevel and longitudinal modeling using Stata : Vol. 1 : Continuous responses. Stata Press, College Station, Tex
67.
go back to reference Cohen J (1988) Statistical power analysis for the behavioral sciences. Laurence Erlbaum, Hillsdale, N. J Cohen J (1988) Statistical power analysis for the behavioral sciences. Laurence Erlbaum, Hillsdale, N. J
68.
go back to reference Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A, Gerard P, Pierelli F, Schoenen J (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1360–1367CrossRefPubMed Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A, Gerard P, Pierelli F, Schoenen J (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1360–1367CrossRefPubMed
69.
go back to reference Hodkinson DJ, Wilcox SL, Veggeberg R, Noseda R, Burstein R, Borsook D, Becerra L (2016) Increased Amplitude of Thalamocortical Low-Frequency Oscillations in Patients with Migraine. J Neurosci 36:8026–8036CrossRefPubMedPubMedCentral Hodkinson DJ, Wilcox SL, Veggeberg R, Noseda R, Burstein R, Borsook D, Becerra L (2016) Increased Amplitude of Thalamocortical Low-Frequency Oscillations in Patients with Migraine. J Neurosci 36:8026–8036CrossRefPubMedPubMedCentral
71.
go back to reference Fuggetta G, Noh NA (2013) A neurophysiological insight into the potential link between transcranial magnetic stimulation, thalamocortical dysrhythmia and neuropsychiatric disorders. Exp Neurol 245:87–95CrossRefPubMed Fuggetta G, Noh NA (2013) A neurophysiological insight into the potential link between transcranial magnetic stimulation, thalamocortical dysrhythmia and neuropsychiatric disorders. Exp Neurol 245:87–95CrossRefPubMed
72.
74.
go back to reference Schmidt S, Naranjo JR, Brenneisen C, Gundlach J, Schultz C, Kaube H, Hinterberger T, Jeanmonod D (2012) Pain ratings, psychological functioning and quantitative EEG in a controlled study of chronic back pain patients. PLoS One 7:e31138CrossRefPubMedPubMedCentral Schmidt S, Naranjo JR, Brenneisen C, Gundlach J, Schultz C, Kaube H, Hinterberger T, Jeanmonod D (2012) Pain ratings, psychological functioning and quantitative EEG in a controlled study of chronic back pain patients. PLoS One 7:e31138CrossRefPubMedPubMedCentral
75.
go back to reference Zambito-Marsala S, Erro R, Bacchin R, Fornasier A, Fabris F, Lo Cascio C, Ferracci F, Morgante F, Tinazzi M (2017) Abnormal nociceptive processing occurs centrally and not peripherally in pain-free Parkinson disease patients: A study with laser-evoked potentials. Parkinsonism Relat Disord 34:43–48CrossRefPubMed Zambito-Marsala S, Erro R, Bacchin R, Fornasier A, Fabris F, Lo Cascio C, Ferracci F, Morgante F, Tinazzi M (2017) Abnormal nociceptive processing occurs centrally and not peripherally in pain-free Parkinson disease patients: A study with laser-evoked potentials. Parkinsonism Relat Disord 34:43–48CrossRefPubMed
76.
go back to reference Schuh-Hofer S, Baumgartner U, Treede RD (2015) Effect of sleep deprivation on the electrophysiological signature of habituation to noxious laser stimuli. Eur J Pain 19:1197–1209CrossRefPubMed Schuh-Hofer S, Baumgartner U, Treede RD (2015) Effect of sleep deprivation on the electrophysiological signature of habituation to noxious laser stimuli. Eur J Pain 19:1197–1209CrossRefPubMed
77.
go back to reference Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, Munafo MR (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14:365–376CrossRefPubMed Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, Munafo MR (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14:365–376CrossRefPubMed
78.
go back to reference Magis D, Vigano A, Sava S, d'Elia TS, Schoenen J, Coppola G (2013) Pearls and pitfalls: electrophysiology for primary headaches. Cephalalgia 33:526–539CrossRefPubMed Magis D, Vigano A, Sava S, d'Elia TS, Schoenen J, Coppola G (2013) Pearls and pitfalls: electrophysiology for primary headaches. Cephalalgia 33:526–539CrossRefPubMed
79.
go back to reference Brighina F, Palermo A, Fierro B (2009) Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine. J Headache Pain 10:77–84CrossRefPubMedPubMedCentral Brighina F, Palermo A, Fierro B (2009) Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine. J Headache Pain 10:77–84CrossRefPubMedPubMedCentral
80.
go back to reference Perchet C, Godinho F, Mazza S, Frot M, Legrain V, Magnin M, Garcia-Larrea L (2008) Evoked potentials to nociceptive stimuli delivered by CO2 or Nd:YAP lasers. Clin Neurophysiol 119:2615–2622CrossRefPubMed Perchet C, Godinho F, Mazza S, Frot M, Legrain V, Magnin M, Garcia-Larrea L (2008) Evoked potentials to nociceptive stimuli delivered by CO2 or Nd:YAP lasers. Clin Neurophysiol 119:2615–2622CrossRefPubMed
81.
go back to reference Rauschel V, Ruscheweyh R, Krafczyk S, Straube A (2016) Test-retest reliability of visual-evoked potential habituation. Cephalalgia 36:831–839CrossRefPubMed Rauschel V, Ruscheweyh R, Krafczyk S, Straube A (2016) Test-retest reliability of visual-evoked potential habituation. Cephalalgia 36:831–839CrossRefPubMed
82.
go back to reference Lisicki M, Ruiz-Romagnoli E, D'Ostilio K, Piedrabuena R, Giobellina R, Schoenen J, Magis D (2016) Familial history of migraine influences habituation of visual evoked potentials. Cephalalgia. doi:10.1177/0333102416673207 Lisicki M, Ruiz-Romagnoli E, D'Ostilio K, Piedrabuena R, Giobellina R, Schoenen J, Magis D (2016) Familial history of migraine influences habituation of visual evoked potentials. Cephalalgia. doi:10.​1177/​0333102416673207​
83.
go back to reference de Tommaso M, Losito L, Libro G, Guido M, Di Fruscolo O, Sardaro M, Sciruicchio V, Lamberti P, Livrea P (2005) Effects of symptomatic treatments on cutaneous hyperalgesia and laser evoked potentials during migraine attack. Cephalalgia 25:359–368CrossRefPubMed de Tommaso M, Losito L, Libro G, Guido M, Di Fruscolo O, Sardaro M, Sciruicchio V, Lamberti P, Livrea P (2005) Effects of symptomatic treatments on cutaneous hyperalgesia and laser evoked potentials during migraine attack. Cephalalgia 25:359–368CrossRefPubMed
84.
go back to reference Schwedt TJ, Krauss MJ, Frey K, Gereau RWt (2011) Episodic and chronic migraineurs are hypersensitive to thermal stimuli between migraine attacks. Cephalalgia 31:6–12CrossRefPubMed Schwedt TJ, Krauss MJ, Frey K, Gereau RWt (2011) Episodic and chronic migraineurs are hypersensitive to thermal stimuli between migraine attacks. Cephalalgia 31:6–12CrossRefPubMed
85.
go back to reference Schwedt TJ, Zuniga L, Chong CD (2015) Low heat pain thresholds in migraineurs between attacks. Cephalalgia 35:593–599CrossRefPubMed Schwedt TJ, Zuniga L, Chong CD (2015) Low heat pain thresholds in migraineurs between attacks. Cephalalgia 35:593–599CrossRefPubMed
86.
go back to reference Engstrom M, Hagen K, Bjork MH, Stovner LJ, Gravdahl GB, Stjern M, Sand T (2013) Sleep quality, arousal and pain thresholds in migraineurs: a blinded controlled polysomnographic study. J Headache Pain 14:12CrossRefPubMedPubMedCentral Engstrom M, Hagen K, Bjork MH, Stovner LJ, Gravdahl GB, Stjern M, Sand T (2013) Sleep quality, arousal and pain thresholds in migraineurs: a blinded controlled polysomnographic study. J Headache Pain 14:12CrossRefPubMedPubMedCentral
87.
go back to reference Burstein R, Cutrer MF, Yarnitsky D (2000) The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain 123(Pt 8):1703–1709CrossRefPubMed Burstein R, Cutrer MF, Yarnitsky D (2000) The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain 123(Pt 8):1703–1709CrossRefPubMed
88.
go back to reference Headache Classification Committee of the International Headache Society (2013) The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 33:629–808 Headache Classification Committee of the International Headache Society (2013) The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 33:629–808
Metadata
Title
Habituation of laser-evoked potentials by migraine phase: a blinded longitudinal study
Authors
Martin Uglem
Petter Moe Omland
Marit Stjern
Gøril Bruvik Gravdahl
Trond Sand
Publication date
01-12-2017
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 1/2017
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1186/s10194-017-0810-6

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